Assignment of Rfp-Y to the chicken major histocompatibility complex/NOR microchromosome and evidence for high-frequency recombination associated with the nucleolar organizer region.

Miller, Marcia M.; Goto, Ronald M.; Taylor, Robert L.; Zoorob, Rima; Auffray, Charles; Briles, R. W.; Briles, W. E.; Bloom, Stephen E.

doi:10.1073/pnas.93.9.3958

Cited by 135 publications

(78 citation statements)

References 33 publications

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“…Overall, the MHC region in chicken stands out in contrast to the MHC in mammals. The chicken MHC is compact and segmented into the MHC-B and MHC-Y regions in which the MHC class I and class II loci reside, as well as genes that changed or moved later in evolutionary time in other species (6,(12)(13)(14)(15). Meiotic recombination within MHC-B is rare (16), but several recombinant haplotypes are available that are suitable for further investigation of MHC-Blinked disease resistance.…”

mentioning

confidence: 99%

BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken

Goto

Wang

Taylor

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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Pathogen selection is postulated to drive MHC allelic diversity at loci for antigen presentation. However, readily apparent MHC infectious disease associations are rare in most species. The strong link between MHC- B haplotype and the occurrence of virally induced tumors in the chicken provides a means for defining the relationship between pathogen selection and MHC polymorphism. Here, we verified a significant difference in resistance to gallid herpesvirus-2 (GaHV-2)-induced lymphomas (Marek's disease) conferred by two closely-related recombinant MHC- B haplotypes. We mapped the crossover breakpoints that distinguish these haplotypes to the highly polymorphic BG1 locus. BG1 encodes an Ig-superfamily type I transmembrane receptor-like protein that contains an immunoreceptor tyrosine-based inhibition motif (ITIM), which undergoes phosphorylation and is recognized by Src homology 2 domain-containing protein tyrosine phosphatase (SHP-2). The recombinant haplotypes are identical, except for differences within the BG1 3′-untranslated region (3′-UTR). The 3′-UTR of the BG1 allele associated with increased lymphoma contains a 225-bp insert of retroviral origin and showed greater inhibition of luciferase reporter gene translation compared to the other allele. These findings suggest that BG1 could affect the outcome of GaHV-2 infection through modulation of the lymphoid cell responsiveness to infection, a condition that is critical for GaHV-2 replication and in which the MHC- B haplotype has been previously implicated. This work provides a mechanism by which MHC- B region genetics contributes to the incidence of GaHV-2-induced malignant lymphoma in the chicken and invites consideration of the possibility that similar mechanisms might affect the incidence of lymphomas associated with other oncogenic viral infections.

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mentioning

confidence: 99%

BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken

Goto

Wang

Taylor

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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“…The same feature is found for the Xenopus MHC, in which only one class I gene of the classical type is MHC linked (49), while a large set of linked nonclassical class I genes is found in another gene complex half a chromosome away (50,51). In chickens, two class I genes (one highly expressed) sandwich the TAP1 and TAP2 genes, and Kaufman and colleagues (11,21,52) have proposed that the tight linkage has allowed the particular class I and TAP alleles to coevolve; furthermore, like in frogs, several nonclassical chicken class I genes are found a great distance away from the true MHC on the same chromosome (53). In the banded houndshark Triakis scyllium, there are one or two classical class I genes depending on the haplotype examined (54), and the majority of teleost species examined rigorously (except cod (29) and cichlid (25,26)) have relatively few class I genes in the class I region.…”

Section: Figure 11mentioning

confidence: 99%

Proteasome, Transporter Associated with Antigen Processing, and Class I Genes in the Nurse SharkGinglymostoma cirratum: Evidence for a Stable Class I Region and MHC Haplotype Lineages

Ohta

McKinney

Criscitiello

et al. 2002

The Journal of Immunology

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Cartilaginous fish (e.g., sharks) are derived from the oldest vertebrate ancestor having an adaptive immune system, and thus are key models for examining MHC evolution. Previously, family studies in two shark species showed that classical class I (UAA) and class II genes are genetically linked. In this study, we show that proteasome genes LMP2 and LMP7, shark-specific LMP7-like, and the TAP1/2 genes are linked to class I/II. Functional LMP7 and LMP7-like genes, as well as multiple LMP2 genes or gene fragments, are found only in some sharks, suggesting that different sets of peptides might be generated depending upon inherited MHC haplotypes. Cosmid clones bearing the MHC-linked classical class I genes were isolated and shown to contain proteasome gene fragments. A non-MHC-linked LMP7 gene also was identified on another cosmid, but only two exons of this gene were detected, closely linked to a class I pseudogene (UAA-NC2); this region probably resulted from a recent duplication and translocation from the functional MHC. Tight linkage of proteasome and class I genes, in comparison with gene organizations of other vertebrates, suggests a primordial MHC organization. Another nonclassical class I gene (UAA-NC1) was detected that is linked neither to MHC nor to UAA-NC2; its high level of sequence similarity to UAA suggests that UAA-NC1 also was recently derived from UAA and translocated from MHC. These data further support the principle of a primordial class I region with few class I genes. Finally, multiple paternities in one family were demonstrated, with potential segregation distortions.

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“…Rfp-Y was detected initially when two sets of polymorphic restriction fragments revealed by B system class I and class II probes were found to assort independently of one another in families of fully pedigreed animals (13). Rfp-Y was later found to correspond to the cosmid clusters II/IV and III in the molecular map (19) of chicken MHC genes (14,15).…”

Section: Hla-e -F -G H Imentioning

confidence: 99%

“…Also mapping to chromosome 16 is the single nucleolar organizer region found within the chicken genome (17) and a single nonpolymorphic classical class II␣ locus (18). A chromosomal region supporting highly frequent meiotic recombination, perhaps associated with the nucleolar organizer region, separates B and Rfp-Y such that the two clusters are genetically unlinked even though they are located on the same microchromosome (15,16). This arrangement is quite different from the arrangement of class I loci in the mouse into H-2K and H-2D where the loci remain linked despite physical separation.…”

Section: Hla-e -F -G H Imentioning

confidence: 99%

“…Restriction fragment pattern-Y (Rfp-Y) and B are two genetically independent clusters of MHC class I and class II␤ genes in the chicken that map to a single microchromosome (chromosome 16) (13)(14)(15)(16). Also mapping to chromosome 16 is the single nucleolar organizer region found within the chicken genome (17) and a single nonpolymorphic classical class II␣ locus (18).…”

Section: Hla-e -F -G H Imentioning

confidence: 99%

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At Least One Class I Gene in Restriction Fragment Pattern-Y (Rfp-Y), the SecondMHCGene Cluster in the Chicken, Is Transcribed, Polymorphic, and Shows Divergent Specialization in Antigen Binding Region

Afanassieff

Goto

et al. 2001

The Journal of Immunology

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MHC genes in the chicken are arranged into two genetically independent clusters located on the same chromosome. These are the classical B system and restriction fragment pattern-Y (Rfp-Y), a second cluster of MHC genes identified recently through DNA hybridization. Because small numbers of MHC class I and class II genes are present in both B and Rfp-Y, the two clusters might be the result of duplication of an entire chromosomal segment. We subcloned, sequenced, and analyzed the expression of two class I loci mapping to Rfp-Y to determine whether Rfp-Y should be considered either as a second, classical MHC or as a region containing specialized MHC-like genes, such as class Ib genes. The Rfp-Y genes are highly similar to each other (93%) and to classical class Ia genes (73% with chicken B class I; 49% with HLA-A). One locus is disrupted and unexpressed. The other, YFV, is widely transcribed and polymorphic. Mature YFV protein associated with β2m arrives on the surface of chicken B (RP9) lymphoma cells expressing YFV as an epitope-tagged transgene. Substitutions in the YFV Ag-binding region (ABR) occur at four of the eight highly conserved residues that are essential for binding of peptide-Ag in the class Ia molecules. Therefore, it is unlikely that Ag is bound in the YFV ABR in the manner typical of class Ia molecules. This ABR specialization indicates that even though YFV is polymorphic and widely transcribed, it is, in fact, a class Ib gene, and Rfp-Y is a region containing MHC genes of specialized function.

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Assignment of Rfp-Y to the chicken major histocompatibility complex/NOR microchromosome and evidence for high-frequency recombination associated with the nucleolar organizer region.

Cited by 135 publications

References 33 publications

BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken

BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken

Proteasome, Transporter Associated with Antigen Processing, and Class I Genes in the Nurse SharkGinglymostoma cirratum: Evidence for a Stable Class I Region and MHC Haplotype Lineages

At Least One Class I Gene in Restriction Fragment Pattern-Y (Rfp-Y), the SecondMHCGene Cluster in the Chicken, Is Transcribed, Polymorphic, and Shows Divergent Specialization in Antigen Binding Region

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